22 Consciousness
- It is a robust general principle of neural dynamics that two
neurons stimulating a third will have a greater total effect
if both their pulses reach the target at the same time (within
some small window of tolerance). From this it follows that
synchronous firing would enhance the neural visibility and
associative power of the disparate components of a cluster.
Binding via synchrony could thus explain why a visual
field containing the same set of features will call up differ-
ent associations depending on how they are grouped—so,
for example, seeing a purple Volkswagen might bring up
memories of an old friend while seeing a purple Ford next
to a green Volkswagen would not. - Neurons in many areas can exhibit oscillatory firing pat-
terns. Phase-locking such oscillations—coordinating them
so their peaks coincide—would be a powerful and effi-
cient means of generating synchrony across large dis-
tances in cortex. The need for a mechanism of synchrony
would thus provide one (though by no means the only)
possible explanation for the ubiquity of these oscillatory
firing patterns.
The details of empirical studies on synchrony are beyond
the scope of this chapter, but it is now widely accepted that
synchronous oscillation plays an important role in visual
binding and may also be crucial for attentional processes and
working memory (for review and discussion, see Engel,
Fries, Konig, Brecht, & Singer, 1999; Engel & Singer, 2001).
Synchrony can thus be considered at least a neural precon-
dition for consciousness because conscious attention and
awareness operate within the realm of whole, bound objects
(Treisman & Kanwisher, 1998).
Christof Koch and Francis Crick advanced a more specific
proposal, which has come to be known as the40-Hz hypothe-
sis(Koch & Crick, 1994). The central idea of this proposal
was that synchronous oscillation in the so-called “gamma
band” frequency range (approximately 25–55 Hz) is both nec-
essary and sufficient for consciousness—in other words, that
we are conscious of the representational contents of all
neurons synchronously oscillating in this frequency band, and
that all our conscious imagery is accompanied by such
oscillations.
The 40-Hz hypothesis was a breakthrough in two respects.
First, it led directly to clear, empirically testable claims about
the neural correlate of consciousness (NCC). At the single-
cell level, the hypothesis implies that the activity of a given
sensory neuron should match the contents of sensory con-
sciousness (e.g., in experiments like those of Logothetis men-
tioned earlier) whenever it is oscillating at frequencies in the
gamma band. At the level of functional areas, it also follows
that consciousness should be insensitive to differences in
activity that are restricted to areas that do not exhibit signifi-
cant gamma-band oscillation. This latter idea was the basis
for the famous conjecture that we are not conscious of the
contents of V1, the first stage of processing in visual cortex
(Crick & Koch, 1995). Unfortunately, as Crick and Koch
themselves pointed out, complicating factors render these
seemingly simple implications problematic: How can one
distinguish the neurons that are driving an oscillation from
those that are merely responding to it? What about local in-
hibitory neurons, which play no direct role in communicating
with other cortical areas—should they be considered part
of the NCC if they oscillate? In recognition of these com-
plexities, Crick and Koch now assume that the anatomical
side of the NCC story will be more complex, involving (at
minimum) finer-grained analysis of the contributions of dif-
ferent cell types and cortical layers (Crick & Koch, 1998).
The original 40-Hz hypothesis was novel in a second way
that has been less widely noticed but may ultimately have
more lasting consequences: Unlike previous synchrony mod-
els of binding, it provided a way to draw a distinction within
the realm of bound representations, between those which are
and are not conscious. If the 40-Hz hypothesis was correct, a
neuroscientist observing the activity of a pair of sensory neu-
rons in separate areas could place them into one of three cat-
egories based solely on the properties of their spike trains:- If oscillating synchronously in the gamma band, the
neurons must be contributing to a single conscious
representation. - If oscillating synchronously at a frequency outsidethe
gamma band, they must be part of a bound representation
that is notpresent to consciousness (e.g., an object in an
unattended part of the visual field). - If active but not oscillating or oscillating out of synchrony,
they must be representing features which are unbound, or
perhaps bound to different representations.
Even though 40-Hz oscillation itself is looking less attrac-
tive as a criterion, it would clearly be useful to have some
means of drawing this distinction between bound representa-
tions that are and are not conscious, and another candidate for
this role is discussed in the next section.Thalamocortical LoopsThe thalamus is a lower forebrain structure that is sometimes
referred to as the gateway to the brain because all sensory sig-
nals except olfaction must pass through it to get to the cortex.
The cortex also projects profusely back to the thalamus;
for many thalamic nuclei, these downward projections